Population biology of the gastropod Olivella minuta (Gastropoda,Olividae) on two sheltered beaches in southeastern Brazil

Marcelo Petracco*, Rita Monteiro Camargo, Daniel Teixeira Tardelli, Alexander TurraDepto. Oceanogra!a Biológica, Instituto Oceanográ!co, Universidade de São Paulo (USP), Praça do Oceanográ!co, 191, Cidade Universitária, São Paulo CEP05508-120, SP, Brazil

a r t i c l e i n f o

Article history:Received 11 December 2012Accepted 17 October 2013Available online 25 October 2013

Keywords:benthosbeachesgastropodintraspeci!c relationshipspopulation dynamics

a b s t r a c t

The structure, dynamics and production of two populations of the olivid gastropod Olivella minuta wereanalyzed through monthly sampling from November 2009 through October 2011 on two sandy beaches,Pernambuco (very sheltered) and Barequeçaba (sheltered) in São Paulo state (23!48’S), southeasternBrazil. On both beaches, samples were taken along !ve transects established perpendicular to thewaterline. Parameters of the von Bertalanffy growth function were estimated for both populations frommonthly length-frequency distributions. The production and turnover ratios were determined using themass-speci!c growth rate method. The population on the less-sheltered Barequeçaba Beach was lessabundant (120.02 " 22.60 ind m#1) than on Pernambuco Beach (3295.30 " 504.86 ind m#1 ("SE)), whichwe attribute to the greater environmental stability of the latter. Conversely, the mean length, size of thelargest individual, and body mass were higher at Barequeçaba than at Pernambuco. The signi!cantdifferences in the growth of individuals and the mortality rate (Z) between the beaches suggest thatdensity-dependent processes were operating at Pernambuco Beach. The production and P/B ratio atPernambuco (12.12 g AFDM m#1 year#1 and 1.91 year#1) were higher than at Barequeçaba(0.82 g AFDM m#1 year#1 and 1.06 year#1). The difference in production can be attributed to the higherabundance on Pernambuco, while the higher P/B ratio resulted from the scarcity of smaller individuals inthe intertidal zone of Barequeçaba. The P/B ratio estimated for the Pernambuco population is the highestfound so far for sandy-beach gastropods. This study reinforces the theory that biological interactions areimportant regulators of sheltered sandy-beach populations. Future studies with multi-beach samplingare needed to better understand the life-history variations of O. minuta along gradients of degree ofexposure of sandy beaches.

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1. Introduction

In the last decade, several studies have examined life-historytraits of macrofauna populations in relation to different physicalfactors of sandy beaches. These studies were conductedmainly withcrustaceans that live in the intertidal and supralittoral zones ofexposed sandy beaches with different morphodynamic states(Gómez and Defeo, 1999; Defeo et al., 2001; Defeo and Martínez,2003; Celentano and Defeo, 2006; Celentano et al., 2010; Defeoand McLachlan, 2011). The studies found marked differencesin population structure and dynamics according to the beachmorphodynamics. In general, the abundance, growth and survivalrate of intertidal species increase from beaches with a more

rigorous morphodynamic state (re"ective) to a more benign state(dissipative), while supralittoral populations follow an inversepattern (Defeo andGómez, 2005; Defeo andMcLachlan, 2005, 2011).

In contrast to the considerable knowledge regarding the popu-lation ecology of the macrofauna of exposed sandy beaches (seeDefeo and McLachlan, 2005), the study of the life-history traits ofsheltered sandy-beach macrofauna is a historically neglected areaof sandy-beach ecology (Cardoso et al., 2011; Mattos and Cardoso,2012). Recently, a few studies have addressed the population dy-namics of macrofauna species on sheltered sandy beaches, most ofthem mollusks in southeastern Brazil (e.g., Denadai et al., 2004;Yokoyama, 2010; Mattos and Cardoso, 2012; Cabrini and Cardoso,2012). However, there is no information on how the populationparameters of mollusks respond to different degrees of exposure ofthe beaches (e.g., very sheltered versus sheltered sandy beaches).

Gastropod mollusks are important components of the mac-rofauna of sheltered sandy beaches, generally as predators and/or

* Corresponding author.E-mail addresses: mpetracco@uol.com.br, marcelopetracco@gmail.com

(M. Petracco).

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Estuarine, Coastal and Shelf Science 150 (2014) 149e156

scavengers (Amaral et al., 2003; Denadai et al., 2005; McLachlanand Brown, 2006). Olivid gastropods inhabit sandy shores intropical and subtropical regions of the world (Petuch andSargent, 1986) and a few species occur in the cooler seas ofsouthern Australia and New Zealand (Smith, 1998). The olividOlivella minuta is widely distributed, occurring in Texas, WestIndies, eastern Colombia, Venezuela, and from Suriname to Brazil(Ceará to Santa Catarina states) (Rios, 1994). This species inhabitsdiverse coastal environments including exposed and shelteredsandy beaches, tidal "ats, and estuaries (Boehs et al., 2004;Denadai et al., 2005; Rocha-Barreira et al., 2005; Viana et al.,2005; Rolemberg et al., 2008). The population ecology ofO. minuta has not been studied and available information isrestricted to its occurrence in communities (Severeyn et al.,2003; Boehs et al., 2004), the use of its shell by hermit crabs(Turra and Denadai, 2004), morphology and systematics (Marcusand Marcus, 1959), feeding behavior (Arruda et al., 2003), andspatial distribution (Arruda and Amaral, 2003).

Considering that very sheltered and sheltered beaches (a less-benign environment) differ in their hydrodynamic characteristics,differences in demography and in life-history traits are expected forintertidal macrofauna populations. The presence of Olivella minutain the intertidal zone of sheltered beaches with different degrees ofexposure on the northern coast of São Paulo provides an oppor-tunity to study the variability of the population structure and dy-namics in different environments. This study compared thedemography, life-history traits and production of two populationsinhabiting sandy beaches with different degrees of exposure.

2. Material and methods

2.1. Study area

Pernambuco (23!4805400S, 45!2402600W) and Barequeçaba(23!4904300S, 45!2600200 W) beaches border the São SebastiãoChannel on the northern coast of São Paulo state, southeasternBrazil (Fig. 1). Pernambuco is a very sheltered beach (sensuMcLachlan, 1980) situated in the inner part of Araçá Bay. This beachis around 100 mwide, with an extensive intertidal zone (w130 m),a very gentle slope (<1!) and !ne sand with gravel and a highorganic-matter content (w2%) (Nucci et al., 2001; Denadai, 2001).The occurrence of very low waves in Pernambuco, despite themicrotidal regime in this region (w1.5 m), results in a characteristictide-dominated beach with a narrow, coarser-grained, high-tidebeach, fronted by awide, very low-gradient, !ner-grained intertidal"at (sensu Short, 1996, 2006). The macrofauna of this beach is moreabundant and species-rich than on Barequeçaba (Nucci et al., 2001;Amaral et al., 2003; Denadai et al., 2005). Barequeçaba is a shel-tered beach, about 1200 m long with a 100 m-wide intertidal zone,a gentle slope (w1!), and sediment composed of !ne and very !nesand with a low organic-matter content (w0.75%) (Nucci et al.,2001; Amaral et al., 2003; Denadai et al., 2005). Pernambuco hasa signi!cantly higher sand water content than Barequeçaba Beach(Petracco, unpublished data). During the study period, the monthlyprecipitation in São Sebastião municipality ranged from 5 mm (July2011) to 212e280 mm (February 2011 and December 2009), with amean of 112.95 mm" 15.35 (SE). The seawater temperature ranged

Fig. 1. Study area and location of Pernambuco and Barequeçaba beaches.

M. Petracco et al. / Estuarine, Coastal and Shelf Science 150 (2014) 149e156150

from 20.0 (July 2011) to 27.1 !C (February 2011) with a mean of23.4 !C " 0.45 (SE) (CEBIMar e USP).

2.2. Sampling and laboratory procedures

Samples were taken monthly during spring low tides, fromNovember 2009 through October 2011. Five transects perpendic-ular to the waterline were established randomly within a segmentof 100 m on each beach. On Pernambuco Beach, the transectscovered the entire range of distribution of this species in theintertidal zone (w130 m), as determined from pilot samples. OnBarequeçaba Beach, the transects were placed from thewaterline tothe middle intertidal zone, covering a length of 44 m, since Olivellaminuta occurs in the middle/lower intertidal on this beach, asobserved in pilot samples. Because of these differences in width,the sampling units were spaced 4 m apart at Barequeçaba Beachand 12 m apart at Pernambuco Beach along each transect. Thesediment was sampled in quadrats de!ned with a metal square(50 cm on a side) and to a depth of 10 cm. The samples were sievedthrough a 1.0 mm mesh, and the gastropods retained were pre-served in 70% ethanol. The use of 1.0 mm mesh was necessarybecause of the great dif!culty encountered in washing the samplescollected on Pernambuco Beach through a 0.5mmmesh, because ofthe high percentage of silt and abundant stone fragments, gravel,algae and tanaidacean tubes in the sediment. For logistical reasons,no samples of O. minuta were collected in August 2011. The shelllength of the individuals was measured using a stereomicroscope,and the individuals were grouped into 0.5 mm length classes.

To obtain the ash-free dry mass, individuals from Barequeçaba(40) and Pernambuco (69) beaches were dried at 70 !C to constantmass, to measure the dry mass (DM). Ash mass (AM) was obtainedafter burning the dried individuals in a muf"e furnace for 5 h at500 !C. Ash-free dry mass (AFDM) was calculated by subtractingthe ash mass from the dry mass. The procedure for obtaining theAFDM was performed using individuals with the shell, sincesmaller individuals of Olivella minuta are too small to remove thesoft parts from inside the shell without the loss of some tissue.

2.3. Data analysis

2.3.1. Abundance, size structure and length-mass relationshipSpecies abundancewasdeterminedbynumberof individuals per

strip transect (IST: ind m#1), according to Defeo (1998). A two-wayANOVA was used to test the null hypothesis of no signi!cant dif-ference in the abundance of Olivella minuta among months andbetween beaches. To evaluate the size structure of these pop-ulations, the normal components in the length-frequency distribu-tion (LFDs groupedper 0.5mm)were identi!ed and separated usingthe Bhattacharyamethod and a separation index> 2 as the criterionto separate contiguous normal components (Gayanilo et al., 1996;Defeo and Cardoso, 2004). Student’s t-test was used to comparethe overall shell length between Barequeçaba and Pernambuco.

The relationship between length and ash-free dry mass (AFDM) forboth populationswas estimated by the power functionM$ aLb, whereM is theash-freedrymassper individual (gAFDM),L is theshell lengthofthe size class (mm), and a and b are constants. An analysis of covariance(ANCOVA) was employed to compare the length-mass relationshipbetweenthepopulations,using lengthascovariate.Datawere linearized(log-transformed) in order to ful!ll ANCOVA assumptions.

2.3.2. Growth, growth performance, mortality and life spanThe growth parameters of Olivella minuta on the beaches were

estimated by analyzing the monthly length-frequency distribu-tions, following the procedure described by Gómez and Defeo(1999) and Defeo et al. (2001). For each month, normally

distributed components of length-frequencies were separated byapplying the NORMSEP routine (Gayanilo et al., 1996). Next, a valuefor absolute age was assigned to the respective cohorts (lengths)from time zero or birth, to obtain an age-length key. Time zero(t $ 0) was de!ned as the minimum length of recruits found onPernambuco Beach (1.50 mm). The beginning of the age-length keyfor the Barequeçaba population was estimated from data for thePernambuco population because of the absence of smaller in-dividuals at Barequeçaba. The age-length key obtained for bothpopulations was used to !t the von Bertalanffy growth function forseasonality (VBGF: Somers, 1988; Gárcia-Berthou et al., 2012) bynon-linear least squares:Lt $ LN%1# exp% # k%t # t0& # St' St0&&;with S%t& $ %CK=2p&sin%2p%t # ts&&;and St0 $ %CK=2p&sin%2p%t0 # ts&&

where Lt is length at time t (mm); LN is the theoretical maximumlength attained by the species; K is the curvature parameter; Caccounts for the intensity of seasonal growth oscillations; to is thetheoretical age at zero length; ts is the beginning of the sinusoidgrowth oscillation; and WP is the winter-point, i.e., period ofgrowth reduction, expressed as a decimal fraction of the year(WP $ ts ' 0.5). To compare the VBGFs !tted for each beach, ananalysis of the residual sum of squares (ARSS) was performed (Chenet al., 1992; Gómez and Defeo, 1999). The growth index phi prime(f0), de!ned as: f0 $ 2log10 (LN) ' log10K (Pauly and Munro, 1984),was employed to measure growth performance.

The instantaneous mortality rate (Z) was calculated for the twopopulations by the single negative exponential model, using thelength-converted catch curve method (Pauly et al., 1995) of theFISAT program (Gayanilo et al., 1996). The estimate of Z was givenby: ln (N) $ g # Z$t, where N is the number of individuals; g theregression intercept; Z, in module, the unbiased estimated mor-tality; and t is the estimated age in each cohort (Pauly et al., 1995).To compare the instantaneous mortality rate between populations,an ANCOVA was employed using age as the covariate. Life span(tmax) was estimated using the length representing the 99thpercentile of the population, L99% (Sparre et al., 1989).

2.3.3. Secondary productionSomatic production of the two populations (P) was estimated by

the mass-speci!c growth rate method (MSGRM: Crisp, 1984; Brey,2001). In this method the production is calculated from thelength-frequency distribution obtained from all pooled samples,the length-mass relationship, and the von Bertalanffy growthfunction parameters. The annual production is given by the equa-tion: P $ SSfi$mi$Gi, where fi is the annual mean number of in-dividuals in length-class i,mi is the mean individual mass in length-class i, calculated from the mean length in length-class i, and Gi isthemass-speci!c growth rate in length-class i obtained through theequation: Gi $ b$K$[(LN/Li) # 1], where b is the exponent of thelength-mass relationship, K and LN are von Bertalanffy growthefunction parameters, and Li is the mean length in length-class i.Production was expressed in running meters (g m#1 year#1) andalso in square meters (g m#2 year#1) to enable comparison withother studies of production. The P/B ratio was calculated by theratio between somatic production (P) and mean biomass (B).

3. Results

3.1. Abundance, across-shore distribution, size structure andlength-mass relationship

The mean abundance of Olivella minuta in Pernambuco(3295.30 " 504.86 ind m#1 ("SE)) was signi!cantly higher than in

M. Petracco et al. / Estuarine, Coastal and Shelf Science 150 (2014) 149e156 151

Barequeçaba (120.02 " 22.60 ind m#1) (ANOVA F1,1 $ 230.85,p< 0.0001). The populations varied in abundance between months(ANOVA F1,22 $ 23.61, p < 0.0001) and the interaction between thefactors beaches and months showed that the variation of theabundance, although following a very clear cyclic pattern withreduction/absence of these gastropods in February/March in bothbeaches, differed between the beaches (ANOVA F1,22 $ 8.45,p < 0.0001) (Fig. 2a). On Pernambuco Beach, peaks of abundanceoccurred in spring (November 2009 and October 2010) and winter(July 2011), with no individuals in midsummer (February 2010 and2011). On Barequeçaba Beach, the population reached high abun-dances in spring (November and December 2009) and early sum-mer (January 2010), with few or no individuals during the latesummer (February 2010 andMarch 2011), early fall (April 2011) andspring (October 2011). The lower monthly standard error of themonthly mean abundance at Barequeçaba than at Pernambuco wasa function of the lower abundance at Barequeçaba (Fig. 2a).

The across-shore distribution of Olivella minuta on PernambucoBeach showed a marked and recurrent monthly variation along theintertidal zone in both years (Fig. 2b). In mid-spring (November),these gastropods occupied the entire intertidal (ca. 130 m), con-trasting with the distribution in early summer (January), when theywere restricted to the lower intertidal. In midsummer (Februaryand March), few or no individuals were present, and during latesummer and early autumn (March and April), O. minuta recolonizedthe intertidal zone through an across-shore migration from thesubtidal (Fig. 2a, b). In winter (July to September), the gastropodsreturned to occupy the entire intertidal zone of Pernambuco Beach.In both years, a new cohort of smaller individuals (1.0e2.5mm)wasdetected in Pernambuco from winter onward. During the recruit-ment period (August to January), the length-frequency distribu-tions (LFDs) showed a bimodal pattern with two well-de!nedcohorts (Fig. 2b, c). After the period when O. minuta was absentfrom the intertidal (February and March), the cohort of larger in-dividuals (>7 mm), which were probably recruited in the previouswinter/spring, did not return to the intertidal. Thus, a clear

unimodal pattern of the LFDs, with individuals of intermediatelength classes (4e8mm) predominating, appeared fromMarch andApril through July, until a new cohort was detected in August andSeptember. The recruits occurred throughout the intertidal zone,although they were more frequent in the lower levels.

The across-shore distribution of Olivella minuta on Barequeçabashowed noticeable differences from the Pernambuco population(Fig. 2b, c). On Barequeçaba, O. minuta was represented mainly byindividuals larger than 4 mm, and restricted to the intermediate/lower intertidal zone (ca. 36 m wide). The monthly LFDs in Bare-queçabaweremainly unimodal due to the absence of recruits in theintertidal. However, similarly to Pernambuco Beach, the across-shore distribution on Barequeçaba showed marked seasonal vari-ations. After occupying almost the entire intertidal zone during thelate spring and early summer (November to December), the gas-tropods retreated to a narrower range of the lower intertidal in thesubsequent months (February to April), when they were absent orin smaller numbers.

The LFDs obtained for the two years of sampling for the Per-nambuco and Barequeçaba populations were bimodal (Fig. 3 andTable 1). The twomodes of the Barequeçaba populationwere largerthan the two modes of the Pernambuco population. The smallestand largest individuals collected at Barequeçaba (3.5 and 12.3 mm)were larger than at Pernambuco (1.6 and 10.8 mm) (Table 1). Themean length of Olivella minuta at Barequeçaba (8.32 " 0.08 mm)was signi!cantly larger than at Pernambuco (6.07 " 0.12 mm)(t1,204 $ 15.67, p < 0.0001). Similarly, the individual body mass atBarequeçaba was signi!cantly larger than at Pernambuco (shelllength as covariate; ANCOVA F1,106 $ 30.87, p < 0.0001) (Fig. 4).

3.2. Growth, growth performance, mortality, life span andsecondary production

The !tting of the VBGF explained 99% of the variance in bothcases. The growth parameters were signi!cant, except t0 in Bare-queçaba and C in Pernambuco, which were marginally signi!cant

Fig. 2. Olivella minuta. Monthly variations in (a) abundance (ind m#1: mean " SE), (b) across-shore distribution, and (c) length-frequency distribution (mm) at Pernambuco (leftpanels) and Barequeçaba (right panels) beaches from November 2009 through October 2011.

M. Petracco et al. / Estuarine, Coastal and Shelf Science 150 (2014) 149e156152

(p $ 0.05 and p $ 0.06, respectively) (Table 1 and Fig. 5). Theanalysis of growth parameters revealed that Olivella minuta differedsigni!cantly in individual growth between the beaches (ARSSF3,35 $ 3.27, p < 0.05), with a slightly larger asymptotic length (LN)and curvature parameter (K) at Barequeçaba than at Pernambuco.Similarly, the phi prime (f0) value was slightly higher at Bare-queçaba (2.28) than at Pernambuco (2.19). Both populationsshowed moderate seasonal oscillations in individual growth(C $ 0.35 and 0.57), with slower growth (WP) in the summer(February). The instantaneous mortality rate estimated for thePernambuco population (4.50 yr#1) was signi!cantly higher than atBarequeçaba (3.55 yr#1) (ANCOVA, F1,13 $ 12.62, p < 0.01), andconversely, the estimated life span at Pernambuco (1.50 years) wasshorter than at Barequeçaba (1.82 years).

The mean biomass, production and P/B ratio estimated for Oli-vella minuta at Pernambuco were higher than at Barequeçaba(Table 1). Higher values for production followed the peaks ofabundance (Fig. 6a, b). In Barequeçaba the highest peak of pro-duction occurred at 9.5 mm, while in Pernambuco the highestproduction occurred at 7.0mm. In the latter beach the smaller (1.5e3.5 mm) and larger individuals (8.0e10.5 mm) contributed simi-larly to the population production (18 and 15%, respectively).

4. Discussion

Marked differences in abundance, across-shore distribution, andsize structure were observed between the two Olivella minutapopulations. The higher abundance at Pernambuco Beach wasprobably due to the greater environmental stability, with highersand moisture content on this very sheltered beach, than in a lessbenign environment such as the sheltered Barequeçaba Beach(sensu Dexter, 1992). The higher sand moisture content at Per-nambuco and the gentler wave action on this very sheltered beachreinforce this supposition. The presence of individuals, includingnewly settled recruits, throughout the intertidal zone of Pernam-buco supports the hypothesis that the intertidal of this beachmightbe a more favorable environment for O. minuta than the intertidalof Barequeçaba.

The peaks of abundance in some months (e.g., November 2009and October 2010) at Pernambuco Beach were due to intenserecruitment events (Fig. 2a, c). Conversely, the higher abundance atBarequeçaba cannot be attributed directly to recruitment. However,the migration to the intertidal zone of individuals recruited in priorperiods in the infralittoral ((5 mm) was partially responsible forthe variation in abundance in the Barequeçaba intertidal. On theother hand, the recurrent low abundance or absence of the in-dividuals in the intertidal of both beaches was related to migrationto the infralittoral. The importance of migration in affecting thetemporal variation in abundance was evidenced by the positiverelationship between the monthly abundance and the extent of thedistribution across the intertidal of Pernambuco (n $ 23, r $ 0.70,

Table 1Olivella minuta. Biological attributes of Pernambuco and Barequeçaba populations.Smallest individual (SI, mm), largest individual (LI, mm), modal values ("SD) derivedfrom the LFD analysis (mm), asymptotic length (LN, mm); parameter of curvature (K,year#1), constant of seasonal oscillation (C), initial point of seasonal oscillation (ts),age at zero length (t0: year), growth index phi prime (f0), life span (tmax, years),instantaneous mortality rate (Z, year#1), production (P, g AFDM m#1 year#1), meanbiomass (B, g AFDM m#1) and P/B ratio (year#1). Signi!cance level of growth pa-rameters for O. minuta populations: *p < 0.05; ***p < 0.001.

Attributes Pernambuco Barequeçaba

SI 1.60 3.60LI 10.80 12.30Modes 1st 2.48 (0.48) 7.68 (0.65)2nd 7.21 (0.86) 9.43 (0.79)LN 11.16*** 11.43***K 1.25* 1.45*C 0.35 0.57*ts 0.79*** 0.79***t0 #0.10* #0.08R2 0.99 0.99f0 2.19 2.28tmax 1.50 1.82Z 4.50 3.55P 12.12 0.82B 6.33 0.78P/B 1.91 1.06

Fig. 4. Olivella minuta. Length-mass relationship for the Pernambuco and Barequeçabapopulations.

Fig. 5. Olivella minuta. Growth curves !tted for the Pernambuco and Barequeçabapopulations.

Fig. 3. Olivella minuta. Length-frequency distribution from November 2009 throughOctober 2011 at Pernambuco and Barequeçaba beaches.

M. Petracco et al. / Estuarine, Coastal and Shelf Science 150 (2014) 149e156 153

p< 0.0001) and Barequeçaba beaches (n$ 23, r$ 0.71, p< 0.0001).Gastropods frequently migrate both vertically and horizontally tothe beach (e.g., Edwards, 1969; Caetano et al., 2003; Denadai et al.,2004). The migration of sandy-beach macrofauna may be relatedboth to biological factors such as reproductive behavior (e.g., Nodaand Nakao, 1995; Denadai et al., 2004) and to biotic factors such asvariations in temperature, precipitation and beach slope (Caetanoet al., 2003; Defeo and McLachlan, 2005). The migration of Oli-vella minuta seems to be stimulated by increases of seawatertemperature and/or precipitation, since the extent of the distribu-tion of this gastropod across the intertidal of Pernambuco Beachwas negatively related to both these abiotic factors (n $ 23,r $ #0.74 and #0.44, p < 0.05). However, the absence of theserelationships at Barequeçaba suggests that the migration of the twoO. minuta populations may be triggered by different factors.

An increase in mortality of larger individuals due to energyexpenditure during the preceding reproductive period, as observedfor the isopod Excirolana braziliensis by Zuñiga et al. (1985), mayexplain the change of LFDs from bi- to unimodal patterns betweenJanuary and March at Pernambuco (Fig. 2c). Thus, different factorsseem to in"uence the temporal variation in abundance of theseOlivella minuta populations; recruitment, migration, and highmortality of the larger, reproductive individuals.

The size structure of these Olivella minuta populations showedmarked differences between areas. The larger mean length, size ofthe largest individual, and the last mode of LFD at Barequeçaba,compared to their counterparts at Pernambuco suggest that thegrowth rate was higher at the former beach. Similarly, the largermean body mass of O. minuta at Barequeçaba is likely due to thelower density of this population relative to Pernambuco Beach,where the higher density likely promoted density-dependentgrowth due to intraspeci!c competition. Negative relationshipsbetween abundance and mean length and between abundance andindividual body mass have been reported for other species ofsandy-beach macrofauna, such as the crustacean Excirolana armataand the olivid gastropod Olivella biplicata, and indicate density-dependent growth (Edwards, 1969; Defeo et al., 1997). Intraspe-ci!c and interspeci!c competition has been widely reported forpopulations on exposed sandy beaches (Defeo and de Alava, 1995;Defeo et al., 1997, 2001; Brazeiro and Defeo,1999; Lima et al., 2000).Moreover, in more benign environments such as sheltered beaches,biological interactions are even more important than in exposedbeaches (Defeo and McLachlan, 2005). This supposition is based onobservations that biological interactions such as intra-speci!ccompetition are particularly meaningful in exposed dissipativebeaches, which havemore benign physical conditions than exposed

re"ective beaches (Defeo and McLachlan, 2005). Further, despitethe lower abundance at Barequeçaba, the presence of smaller in-dividuals in the subtidal of this beach (Yokoyama et al., 2012)suggests a size-strati!ed distribution, which may reduce intraspe-ci!c competition and thus increase the growth rate and the bodymass for this population, as also observed for O. biplicata (Edwards,1969).

In addition to the differences in population structure, the sig-ni!cant variation in individual growth rates between the beaches,and the slightly higher LN, K and phi prime (f) values at Bare-queçaba, suggest that growth was density-dependent at Pernam-buco, where Olivella minuta was more abundant. Similarly, thehigher mortality rate (Z) and the shorter life span at Pernambucosuggest a density-dependent mortality in this beach. These obser-vations reinforce the importance of intraspeci!c interactions asregulators of the population dynamics of sandy-beach macrofauna.

The moderate decrease in individual growth in the Olivellaminuta populations during the summer may be related to theintense rainfall during this season. However, the absence of in-dividuals at Pernambuco during February and March, and theabsence of smaller individuals at Barequeçaba throughout thestudy period, may have contributed to the estimates of the constantof seasonal oscillation (C) being higher than 0.

The higher estimated production of Olivella minuta at Pernam-buco Beach was due to the higher abundance and biomassobserved. On the other hand, the higher P/B ratio at Pernambucocan be attributed to the strong sample selectivity against smallerindividuals at Barequeçaba, despite the weak representation ofmiddle-sized individuals (3.5e4.5 mm) at Pernambuco, due tomigration (Fig. 2b, c and 3). Although sampling selectivity againstsmaller and middle-sized individuals can led to underestimation ofP/B ratios, and thus to deviations to the relationship of Allen (1971:Z $ P/B), the very sharp differences between Z (3.55e4.50 year#1)and P/B (1.06e1.91 year#1) for the two populations of O. minuta areunexpected. Estimates for higher Z values in relation to the P/Bratios have been recurrent in sandy-beach macrofauna populations(Petracco et al., 2012a, b), and therefore further research is neededto elucidate this important issue.

In contrast to the many production estimates available forbivalve populations (e.g., Herrmann et al., 2009, 2011; Turra et al.,2014), few estimates are available for gastropods of exposed(McLachlan and van der Horst, 1979; Caetano et al., 2003) andsheltered sandy beaches (Denadai et al., 2004; Yokoyama, 2010).Sandy-beach gastropods generally show low production and P/Bratios (Petracco et al., 2013) and generally also show some char-acteristics related to low P/B ratios such as a longer life span

Fig. 6. Olivella minuta. Distribution of production (circles) and abundance (bars) from November 2009 through October 2011 for the (a) Pernambuco and (b) Barequeçabapopulations.

M. Petracco et al. / Estuarine, Coastal and Shelf Science 150 (2014) 149e156154

(Table 2) and low motility (Cusson and Bourget, 2005). However,similarly to the Olivella minuta population of Barequeçaba, availableP/B estimates for other sandy-beach gastropod species such asOlivancillaria vesica and Hastula cinerea are also underestimated,due to the absence of smaller individuals from the intertidal zoneresulting from their size-strati!ed distributions (see Caetano et al.,2003; Petracco, 2008; Petracco et al., 2012b). The P/B ratio calcu-lated for O. minuta at Pernambuco Beach is the highest yet obtainedfor sandy-beach gastropods. This high P/B ratio is due to i) theshorter life span of this population in relation to other gastropodpopulations (Table 2); and ii) the low sample selectivity in thispopulation resulting from the occurrence of smaller individuals inthe intertidal zone.

In summary, several differences were observed between theseOlivella minuta populations inhabiting sheltered sandy beaches.The differences in abundance and in across-shore distribution areattributed to the supposition that the very sheltered sandy beach(Pernambuco) is a more favorable environment for this gastropodthan the sheltered beach (Barequeçaba). The differences in sizestructure, body mass, and growth and mortality rates between thetwo populations suggest that density-dependent processes areoperating at Pernambuco Beach, due to the greater abundance ofthis population. These observations reinforce the theory that bio-logical interactions are important regulators of populations livingin sheltered sandy beaches (benign environments). Future studieswithmulti-beach sampling are crucial for a better understanding ofhow the life-history traits of O. minuta respond to different degreesof exposure of sandy beaches (sheltered-exposed beaches).

Acknowledgments

This paper is part of the M.Sc. dissertation of R.M. Camargo andD.T. Tardelli and of the Postdoctorate of M. Petracco at InstitutoOceanográ!co da Universidade de São Paulo (IOUSP). We wish toexpress our gratitude to all participants in the !eld work (especiallyThayana A. Berenguel) and to CEBIMar (USP) for their logisticassistance. Thanks are due to Dr. Janet W. Reid and to D. T. Ramosfor the English revision. M. Petracco thanks to Dr. Flavio Accursioand Felipe R.P. for their encouragement. This study was supportedby Fundação de Amparo à Pesquisa do Estado de São Paulo, FAPESP(Processes. No. 2008/11053-0; 2010/01426-3; 2010/13589-4; 2009/17585-6).

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Species P B P/B LS Lat Source

Olivancillaria vesica 0.17 0.16 1.06 4.64 23!030S Caetano et al. (2003)Nassarius vibex 0.35 0.90 0.45 4.00 23!370S Yokoyama (2010)Nassarius vibex 3.60 7.98 0.38 5.00 23!370S Yokoyama (2010)Olivella minuta 0.08 0.04 1.91 1.50 23!480S This study (Pernambuco)Olivella minuta 0.02 0.02 1.06 1.82 23!490S This study (Barequeçaba)Hastula cinerea 0.19 0.15 1.28 3.13 24!270S Petracco (2008)Hastula cinerea 0.11 0.16 0.69 4.79 24!270S Petracco (2008)Bullia rhodostoma 0.14 0.17 0.77 10.00 33!570S McLachlan et al. (1979)Bullia rhodostoma 0.58 0.78 0.73 20.00 33!570S McLachlan and van der

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